The heat released during catalytic turnover enhances the diffusion of an enzyme

Riedel, Clement; Gabizon, Ronen; Wilson, Christian A.  M.; Hamadani, Kambiz; Tsekouras, Konstantinos; Marqusee, Susan; Pressé, Steve; Bustamante, Carlos

doi:10.1038/nature14043

Title: The heat released during catalytic turnover enhances the diffusion of an enzyme

Journal Article · Wed Dec 10 00:00:00 EST 2014 · Nature (London)

DOI:https://doi.org/10.1038/nature14043· OSTI ID:1257853

Riedel, Clement ^[1]; Gabizon, Ronen ^[1]; Wilson, Christian A. M. ^[2]; Hamadani, Kambiz ^[1]; Tsekouras, Konstantinos ^[3]; Marqusee, Susan ^[4]; Pressé, Steve ^[5]; Bustamante, Carlos ^[6]

Univ. of California, Berkeley, CA (United States). California Institute for Quantitative Biosciences
Univ. of California, Berkeley, CA (United States). California Institute for Quantitative Biosciences; Univ. of Chile, Santiago (Chile)
Indiana University-Purdue University, Indianapolis, IN (United States)
Univ. of California, Berkeley, CA (United States). California Institute for Quantitative Biosciences; Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology
Indiana University-Purdue University, Indianapolis, IN (United States); Indiana University School of Medicine, IN (United States)
Univ. of California, Berkeley, CA (United States). California Institute for Quantitative Biosciences; Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology; Univ. of California, Berkeley, CA (United States). Jason L. Choy Laboratory of Single-Molecule Biophysics and Department of Physics; Univ. of California, Berkeley, CA (United States). Howard Hughes Medical Institute; Univ. of California, Berkeley, CA (United States). Kavli Energy Nano Sciences Institute

Recent studies have shown that the diffusivity of enzymes increases in a substrate-dependent manner during catalysis. Although this observation has been reported and characterized for several different systems, the precise origin of this phenomenon is unknown. Calorimetric methods are often used to determine enthalpies from enzyme-catalysed reactions and can therefore provide important insight into their reaction mechanisms. The ensemble averages involved in traditional bulk calorimetry cannot probe the transient effects that the energy exchanged in a reaction may have on the catalyst. Here we obtain single-molecule fluorescence correlation spectroscopy data and analyse them within the framework of a stochastic theory to demonstrate a mechanistic link between the enhanced diffusion of a single enzyme molecule and the heat released in the reaction. We propose that the heat released during catalysis generates an asymmetric pressure wave that results in a differential stress at the protein-solvent interface that transiently displaces the centre-of-mass of the enzyme (chemoacoustic effect). We find this novel perspective on how enzymes respond to the energy released during catalysis suggests a possible effect of the heat of reaction on the structural integrity and internal degrees of freedom of the enzyme.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1257853

Journal Information:: Nature (London), Vol. 517, Issue 7533; ISSN 0028-0836

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 156 works

Citation information provided by
Web of Science

References (38)

Enhancement of biomixing by swimming algal cells in two-dimensional films Kurtuldu, H.; Guasto, J. S.; Johnson, K. A. Proceedings of the National Academy of Sciences, Vol. 108, Issue 26 https://doi.org/10.1073/pnas.1107046108	journal	June 2011
Synthetic Mechanochemical Molecular Swimmer Golestanian, Ramin Physical Review Letters, Vol. 105, Issue 1 https://doi.org/10.1103/PhysRevLett.105.018103	journal	June 2010
Calorimetric evaluation of enzyme kinetic parameters Williams, Brent A.; Toone, Eric J. The Journal of Organic Chemistry, Vol. 58, Issue 13 https://doi.org/10.1021/jo00065a010	journal	June 1993
Role of Lys-12 in Catalysis by Triosephosphate Isomerase: A Two-Part Substrate Approach Go, Maybelle K.; Koudelka, Astrid; Amyes, Tina L. Biochemistry, Vol. 49, Issue 25 https://doi.org/10.1021/bi100538b	journal	June 2010
Substrate Catalysis Enhances Single-Enzyme Diffusion Muddana, Hari S.; Sengupta, Samudra; Mallouk, Thomas E. Journal of the American Chemical Society, Vol. 132, Issue 7 https://doi.org/10.1021/ja908773a	journal	February 2010
Isolation and characterization of urease from Aspergillus niger Smith, P. T.; King, A. D.; Goodman, N. Journal of General Microbiology, Vol. 139, Issue 5 https://doi.org/10.1099/00221287-139-5-957	journal	May 1993
Nanoscale swimmers: hydrodynamic interactions and propulsion of molecular machines Sakaue, T.; Kapral, R.; Mikhailov, A. S. The European Physical Journal B, Vol. 75, Issue 3 https://doi.org/10.1140/epjb/e2010-00138-x	journal	May 2010
Protein folding Waller, D. A. Biochemical Education, Vol. 21, Issue 1 https://doi.org/10.1016/0307-4412(93)90022-r	journal	January 1993
Thermodynamics of enzyme-catalyzed reactions--a database for quantitative biochemistry Goldberg, R. N.; Tewari, Y. B.; Bhat, T. N. Bioinformatics, Vol. 20, Issue 16 https://doi.org/10.1093/bioinformatics/bth314	journal	May 2004
Enzyme Kinetics Determined Using Calorimetry: A General Assay for Enzyme Activity? Todd, Matthew J.; Gomez, Javier Analytical Biochemistry, Vol. 296, Issue 2 https://doi.org/10.1006/abio.2001.5218	journal	September 2001
Molecular Propulsion: Chemical Sensing and Chemotaxis of DNA Driven by RNA Polymerase Yu, Hua; Jo, Kyubong; Kounovsky, Kristy L. Journal of the American Chemical Society, Vol. 131, Issue 16 https://doi.org/10.1021/ja900372m	journal	April 2009
Simultaneous pH and Temperature Measurements Using Pyranine as a Molecular Probe Wong, Felix H. C.; Fradin, Cécile Journal of Fluorescence, Vol. 21, Issue 1 https://doi.org/10.1007/s10895-010-0717-y	journal	October 2010
Protein folding Cruzeiro, L. Chemical Modelling https://doi.org/10.1039/9781849730884-00089	book	October 2010
Self-motile colloidal particles: from directed propulsion to random walk Howse, Jonathan R.; Jones, Richard A. L.; Ryan, Anthony J. arXiv https://doi.org/10.48550/arxiv.0706.4406	text	January 2007
Ureases I. Functional, catalytic and kinetic properties: A review Krajewska, Barbara Journal of Molecular Catalysis B: Enzymatic, Vol. 59, Issue 1-3 https://doi.org/10.1016/j.molcatb.2009.01.003	journal	July 2009
Activity and spectroscopic properties of bovine liver catalase in sodium bis(2-ethylhexyl)sulfosuccinate/isooctane reverse micelles Haber, J.; Masalakiewicz, P.; Rodakiewicz-Nowak, J. European Journal of Biochemistry, Vol. 217, Issue 2 https://doi.org/10.1111/j.1432-1033.1993.tb18278.x	journal	October 1993
Conformational Transitions of Adenylate Kinase: Switching by Cracking Whitford, Paul C.; Miyashita, Osamu; Levy, Yaakov Journal of Molecular Biology, Vol. 366, Issue 5 https://doi.org/10.1016/j.jmb.2006.11.085	journal	March 2007
Protein folding Osborn, Thomas Robert Bulletin of the Australian Mathematical Society, Vol. 31, Issue 2 https://doi.org/10.1017/s0004972700004780	journal	April 1985
Diversity of properties among catalases Switala, Jacek; Loewen, Peter C. Archives of Biochemistry and Biophysics, Vol. 401, Issue 2 https://doi.org/10.1016/S0003-9861(02)00049-8	journal	May 2002
Time-resolved photoacoustic calorimetry: probing the energetics and dynamics of fast chemical and biochemical reactions Peters, K.; Snyder, G. Science, Vol. 241, Issue 4869 https://doi.org/10.1126/science.3045967	journal	August 1988
Nanosecond Responses of Proteins to Ultra-High Temperature Pulses Steel, Bradley C.; McKenzie, David R.; Bilek, Marcela M. M. Biophysical Journal, Vol. 91, Issue 6 https://doi.org/10.1529/biophysj.106.090944	journal	September 2006
A catalytically driven organometallic molecular motor Pavlick, Ryan A.; Dey, Krishna K.; Sirjoosingh, Andrew Nanoscale, Vol. 5, Issue 4 https://doi.org/10.1039/C2NR32518G	journal	January 2013
Fluorescence correlation spectroscopy. I. Conceptual basis and theory Elson, Elliot L.; Magde, Douglas Biopolymers, Vol. 13, Issue 1 https://doi.org/10.1002/bip.1974.360130102	journal	January 1974
Thirty years of heme catalases structural biology Díaz, Adelaida; Loewen, Peter C.; Fita, Ignacio Archives of Biochemistry and Biophysics, Vol. 525, Issue 2 https://doi.org/10.1016/j.abb.2011.12.011	journal	September 2012
Fluorescence correlation spectroscopy: the technique and its applications Krichevsky, Oleg; Bonnet, Grégoire Reports on Progress in Physics, Vol. 65, Issue 2 https://doi.org/10.1088/0034-4885/65/2/203	journal	January 2002
Protein folding Kuntz, I. D. Journal of the American Chemical Society, Vol. 94, Issue 11 https://doi.org/10.1021/ja00766a060	journal	May 1972
Can Man-Made Nanomachines Compete with Nature Biomotors? Wang, Joseph ACS Nano, Vol. 3, Issue 1 https://doi.org/10.1021/nn800829k	journal	December 2008
Ferryl intermediates of catalase captured by time-resolved Weissenberg crystallography and UV-VIS spectroscopy Gouet, Patrice; Jouve, Hélène-Marie; Williams, Pamela A. Nature Structural Biology, Vol. 3, Issue 11 https://doi.org/10.1038/nsb1196-951	journal	November 1996
Direct observation of enzyme activity with the atomic force microscope Radmacher, M.; Fritz, M.; Hansma, H. Science, Vol. 265, Issue 5178 https://doi.org/10.1126/science.8079171	journal	September 1994
Protein folding Creighton, T. E. Biochemical Journal, Vol. 270, Issue 1 https://doi.org/10.1042/bj2700001	journal	August 1990
The Enthalpy of Decomposition of Hydrogen Peroxide: A General Chemistry Calorimetry Experiment Marzzacco, Charles J. Journal of Chemical Education, Vol. 76, Issue 11 https://doi.org/10.1021/ed076p1517	journal	November 1999
Self-Motile Colloidal Particles: From Directed Propulsion to Random Walk Howse, Jonathan R.; Jones, Richard A. L.; Ryan, Anthony J. Physical Review Letters, Vol. 99, Issue 4 https://doi.org/10.1103/PhysRevLett.99.048102	journal	July 2007
Enzyme Molecules as Nanomotors Sengupta, Samudra; Dey, Krishna K.; Muddana, Hari S. Journal of the American Chemical Society, Vol. 135, Issue 4 https://doi.org/10.1021/ja3091615	journal	January 2013
A Molecular Thermometer Based on Fluorescent Protein Blinking Wong, Felix H. C.; Banks, Daniel S.; Abu-Arish, Asmahan Journal of the American Chemical Society, Vol. 129, Issue 34 https://doi.org/10.1021/ja0715905	journal	August 2007
Effects of amines and aminoalcohols on bovine intestine alkaline phosphatase activity Sekiguchi, Satoshi; Hashida, Yasuhiko; Yasukawa, Kiyoshi Enzyme and Microbial Technology, Vol. 49, Issue 2 https://doi.org/10.1016/j.enzmictec.2011.04.019	journal	July 2011
Nanorobots: The Ultimate Wireless Self-Propelled Sensing and Actuating Devices Sánchez, Samuel; Pumera, Martin Chemistry - An Asian Journal, Vol. 4, Issue 9 https://doi.org/10.1002/asia.200900143	journal	September 2009
On the Absorption Spectrum of Catalase Stern, Kurt G. Journal of Biological Chemistry, Vol. 121, Issue 2 https://doi.org/10.1016/S0021-9258(18)74288-9	journal	November 1937
A Spectrophotometric Method for Measuring the Breakdown of Hydrogen Peroxide by Catalase Beers, Roland F.; Sizer, Irwin W. Journal of Biological Chemistry, Vol. 195, Issue 1 https://doi.org/10.1016/S0021-9258(19)50881-X	journal	March 1952

Cited By (35)

Universal glass-forming behavior of in vitro and living cytoplasm Nishizawa, Kenji; Fujiwara, Kei; Ikenaga, Masahiro Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-14883-y	journal	November 2017
Fast equilibrium switch of a micro mechanical oscillator Le Cunuder, Anne; Martínez, Ignacio A.; Petrosyan, Artyom Applied Physics Letters, Vol. 109, Issue 11 https://doi.org/10.1063/1.4962825	journal	September 2016
Life in crowded conditions: Molecular crowding and beyond Klumpp, Stefan; Bode, William; Puri, Palka The European Physical Journal Special Topics, Vol. 227, Issue 15-16 https://doi.org/10.1140/epjst/e2018-800088-6	journal	January 2019
Fluctuation correlation spectroscopy and its applications in homogeneous analysis Su, Di; Hou, Yuemei; Dong, Chaoqing Analytical and Bioanalytical Chemistry, Vol. 411, Issue 19 https://doi.org/10.1007/s00216-019-01884-1	journal	June 2019
Enzyme leaps fuel antichemotaxis Jee, Ah-Young; Dutta, Sandipan; Cho, Yoon-Kyoung Proceedings of the National Academy of Sciences, Vol. 115, Issue 1 https://doi.org/10.1073/pnas.1717844115	journal	December 2017
Tracking the rotation of single CdS nanorods during photocatalysis with surface plasmon resonance microscopy Jiang, Yingyan; Su, Hua; Wei, Wei Proceedings of the National Academy of Sciences, Vol. 116, Issue 14 https://doi.org/10.1073/pnas.1820114116	journal	March 2019
Non-invasive perturbations of intracellular flow reveal physical principles of cell organization Mittasch, Matthäus; Gross, Peter; Nestler, Michael Nature Cell Biology, Vol. 20, Issue 3 https://doi.org/10.1038/s41556-017-0032-9	journal	February 2018
Absolute diffusion measurements of active enzyme solutions by NMR Günther, Jan-Philipp; Majer, Günter; Fischer, Peer The Journal of Chemical Physics, Vol. 150, Issue 12 https://doi.org/10.1063/1.5086427	journal	March 2019
Perspective: Watching low-frequency vibrations of water in biomolecular recognition by THz spectroscopy Xu, Yao; Havenith, Martina The Journal of Chemical Physics, Vol. 143, Issue 17 https://doi.org/10.1063/1.4934504	journal	November 2015
Artificial molecular and nanostructures for advanced nanomachinery Ellis, Elizabeth; Moorthy, Suresh; Chio, Weng-I Katherine Chemical Communications, Vol. 54, Issue 33 https://doi.org/10.1039/c7cc09133h	journal	January 2018
Direct Single Molecule Imaging of Enhanced Enzyme Diffusion Xu, Mengqi; Valdez, Lyanne; Sen, Aysuman arXiv https://doi.org/10.48550/arxiv.1811.08483	text	January 2018
Motility of Enzyme-Powered Vesicles Ghosh, Subhadip; Mohajerani, Farzad; Son, Seoyoung bioRxiv https://doi.org/10.1101/645986	posted_content	May 2019
Enhanced Diffusion of Molecular Catalysts is Due to Convection MacDonald, Thomas S. C.; Price, William S.; Astumian, R. Dean Angewandte Chemie, Vol. 131, Issue 52 https://doi.org/10.1002/ange.201910968	journal	November 2019
Mesoscopic non-equilibrium measures can reveal intrinsic features of the active driving Mura, Federica; Gradziuk, Grzegorz; Broedersz, Chase P. Soft Matter, Vol. 15, Issue 40 https://doi.org/10.1039/c9sm01169b	journal	January 2019
Shear viscosity of two-state enzyme solutions Hosaka, Yuto; Komura, Shigeyuki; Andelman, David Physical Review E, Vol. 101, Issue 1 https://doi.org/10.1103/physreve.101.012610	journal	January 2020
Motility of Enzyme-Powered Vesicles Ghosh, Subhadip; Mohajerani, Farzad; Son, Seoyoung Nano Letters, Vol. 19, Issue 9 https://doi.org/10.1021/acs.nanolett.9b01830	journal	August 2019
Dynamic Coupling at Low Reynolds Number Dey, Krishna Kanti Angewandte Chemie International Edition, Vol. 58, Issue 8 https://doi.org/10.1002/anie.201804599	journal	February 2019
Self-Propulsion Strategies for Artificial Cell-Like Compartments Santiago, Ibon; Simmel, Friedrich C. Nanomaterials, Vol. 9, Issue 12 https://doi.org/10.3390/nano9121680	journal	November 2019
An upper limit on Gibbs energy dissipation governs cellular metabolism Niebel, Bastian; Leupold, Simeon; Heinemann, Matthias Nature Metabolism, Vol. 1, Issue 1 https://doi.org/10.1038/s42255-018-0006-7	journal	January 2019
Enzymatically Powered Surface-Associated Self-Motile Protocells Jang, Woo-Sik; Kim, Hyun Ji; Gao, Chen Small, Vol. 14, Issue 36 https://doi.org/10.1002/smll.201801715	journal	August 2018
Topology, landscapes, and biomolecular energy transport Elenewski, Justin E.; Velizhanin, Kirill A.; Zwolak, Michael Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-12700-w	journal	October 2019
Enhanced Diffusion of Molecular Catalysts is Due to Convection MacDonald, Thomas S. C.; Price, William S.; Astumian, R. Dean Angewandte Chemie International Edition, Vol. 58, Issue 52 https://doi.org/10.1002/anie.201910968	journal	December 2019
Dynamische Kopplung bei niedriger Reynoldszahl Dey, Krishna Kanti Angewandte Chemie, Vol. 131, Issue 8 https://doi.org/10.1002/ange.201804599	journal	January 2019
Chemical and hydrodynamic alignment of an enzyme Adeleke-Larodo, T.; Agudo-Canalejo, J.; Golestanian, R. The Journal of Chemical Physics, Vol. 150, Issue 11 https://doi.org/10.1063/1.5081717	journal	March 2019
Catalytic enzymes are active matter Jee, Ah-Young; Cho, Yoon-Kyoung; Granick, Steve Proceedings of the National Academy of Sciences, Vol. 115, Issue 46 https://doi.org/10.1073/pnas.1814180115	journal	November 2018
Enzymes surf the heat wave Wand, A. Joshua Nature, Vol. 517, Issue 7533 https://doi.org/10.1038/nature14079	journal	December 2014
ATP Hydrolysis Induced Conformational Changes in the Vitamin B12 Transporter BtuCD Revealed by MD Simulations Pan, Chao; Weng, Jingwei; Wang, Wenning PLOS ONE, Vol. 11, Issue 11 https://doi.org/10.1371/journal.pone.0166980	journal	November 2016
Langevin Dynamics Driven by a Telegraphic Active Noise Um, Jaegon; Song, Taegeun; Jeon, Jae-Hyung Frontiers in Physics, Vol. 7 https://doi.org/10.3389/fphy.2019.00143	journal	October 2019
Mobility of pectin methylesterase in pectin/cellulose gels is enhanced by the presence of cellulose and by its catalytic capacity Bonnin, Estelle; Alvarado, Camille; Crépeau, Marie-Jeanne Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-49108-x	journal	August 2019
Chemical and hydrodynamic alignment of an enzyme Adeleke-Larodo, Tunrayo; Agudo-Canalejo, Jaime; Golestanian, Ramin arXiv https://doi.org/10.48550/arxiv.1811.09631	text	January 2018
Probing the Spatiotemporal Dynamics of Catalytic Janus Particles with Single-Particle Tracking and Differential Dynamic Microscopy Kurzthaler, Christina; Devailly, Clémence; Arlt, Jochen Physical Review Letters, Vol. 121, Issue 7 https://doi.org/10.1103/physrevlett.121.078001	journal	August 2018
A size-dependent generalized thermoelastic diffusion theory and its application Li, Chenlin; Guo, Huili; Tian, Xiaogeng Journal of Thermal Stresses, Vol. 40, Issue 5 https://doi.org/10.1080/01495739.2017.1300786	journal	November 2016
Topology, Landscapes, and Biomolecular Energy Transport Elenewski, Justin E.; Velizhanin, Kirill A.; Zwolak, Michael arXiv https://doi.org/10.48550/arxiv.1904.11154	text	January 2019
Self-propulsion of catalytic nanomotors synthesised by seeded growth of asymmetric platinum–gold nanoparticles Santiago, Ibon; Jiang, Luyun; Foord, John Chemical Communications, Vol. 54, Issue 15 https://doi.org/10.1039/c7cc09436a	journal	January 2018
Fast equilibrium switch of a micro mechanical oscillator Cunuder, Anne Le; Martinez, Ignacio; Petrosyan, Artyom arXiv https://doi.org/10.48550/arxiv.1606.02453	text	January 2016

Similar Records

Caught before Released: Structural Mapping of the Reaction Trajectory for the Sofosbuvir Activating Enzyme, Human Histidine Triad Nucleotide Binding Protein 1 (hHint1)

Journal Article · Mon Jul 10 00:00:00 EDT 2017 · Biochemistry · OSTI ID:1257853

Shah, Rachit; Maize, Kimberly M.; Zhou, Xin; +2 more

Endoperoxide formation by an α-ketoglutarate-dependent mononuclear non-haem iron enzyme

Journal Article · Mon Nov 02 00:00:00 EST 2015 · Nature (London) · OSTI ID:1257853

Yan, Wupeng; Song, Heng; Song, Fuhang; +12 more

Organic and Organometallic Chemistry at the Single-Molecule, -Particle, and -Molecular-Catalyst-Turnover Level by Fluorescence Microscopy

Journal Article · Tue Jul 16 00:00:00 EDT 2019 · Accounts of Chemical Research · OSTI ID:1257853

Easter, Quinn T.; Blum, Suzanne A.

Related Subjects

60 APPLIED LIFE SCIENCES

Title: The heat released during catalytic turnover enhances the diffusion of an enzyme

Citation Formats

References (38)

Cited By (35)

Similar Records

Related Subjects